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Markert S.,Institute of Marine Biotechnology | Gardebrecht A.,University of Greifswald | Felbeck H.,University of California at San Diego | Sievert S.M.,Woods Hole Oceanographic Institution | And 9 more authors.
Proteomics | Year: 2011

Riftia pachyptila, the giant deep-sea tube worm, inhabits hydrothermal vents in the Eastern Pacific ocean. The worms are nourished by a dense population of chemoautotrophic bacterial endosymbionts. Using the energy derived from sulfide oxidation, the symbionts fix CO 2 and produce organic carbon, which provides the nutrition of the host. Although the endosymbionts have never been cultured, cultivation-independent techniques based on density gradient centrifugation and the sequencing of their (meta-) genome enabled a detailed physiological examination on the proteomic level. In this study, the Riftia symbionts' soluble proteome map was extended to a total of 493 identified proteins, which allowed for an explicit description of vital metabolic processes such as the energy-generating sulfide oxidation pathway or the Calvin cycle, which seems to involve a reversible pyrophosphate-dependent phosphofructokinase. Furthermore, the proteomic view supports the hypothesis that the symbiont uses nitrate as an alternative electron acceptor. Finally, the membrane-associated proteome of the Riftia symbiont was selectively enriched and analyzed. As a result, 275 additional proteins were identified, most of which have putative functions in electron transfer, transport processes, secretion, signal transduction and other cell surface-related functions. Integrating this information into complex pathway models a comprehensive survey of the symbiotic physiology was established. © 2011 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.


Gilbert J.A.,Argonne National Laboratory | Gilbert J.A.,University of Chicago | Meyer F.,Argonne National Laboratory | Meyer F.,University of Chicago | And 16 more authors.
Standards in Genomic Sciences | Year: 2010

This report details the outcome the first meeting of the Earth Microbiome Project to discuss sample selection and acquisition. The meeting, held at the Argonne National Laboratory on Wednesday October 6 th 2010, focused on discussion of how to prioritize environmental samples for sequencing and metagenomic analysis as part of the global effort of the EMP to systematically determine the functional and phylogenetic diversity of microbial communities across the world.


Wu M.L.,Radboud University Nijmegen | Van Teeseling M.C.F.,Radboud University Nijmegen | Willems M.J.R.,Radboud University Nijmegen | Van Donselaar E.G.,University Utrecht | And 8 more authors.
Journal of Bacteriology | Year: 2012

"Candidatus Methylomirabilis oxyfera" is a newly discovered denitrifying methanotroph that is unrelated to previously known methanotrophs. This bacterium is a member of the NC10 phylum and couples methane oxidation to denitrification through a newly discovered intra-aerobic pathway. In the present study, we report the first ultrastructural study of "Ca. Methylomirabilis oxyfera" using scanning electron microscopy, transmission electron microscopy, and electron tomography in combination with different sample preparation methods. We observed that "Ca. Methylomirabilis oxyfera" cells possess an atypical polygonal shape that is distinct from other bacterial shapes described so far. Also, an additional layer was observed as the outermost sheath, which might represent a (glyco)protein surface layer. Further, intracytoplasmic membranes, which are a common feature among proteobacterial methanotrophs, were never observed under the current growth conditions. Our results indicate that "Ca. Methylomirabilis oxyfera" is ultrastructurally distinct from other bacteria by its atypical cell shape and from the classical proteobacterial methanotrophs by its apparent lack of intracytoplasmic membranes. © 2012, American Society for Microbiology.


Aquilina A.,Organic Geochemistry Unit | Aquilina A.,UK National Oceanography Center | Knab N.J.,MPI for Marine Microbiology | Knittel K.,MPI for Marine Microbiology | And 10 more authors.
Organic Geochemistry | Year: 2010

The anaerobic oxidation of methane (AOM) is a major methane sink in marine sediments and plays a crucial role in mitigating methane fluxes to the overlying water column. We investigated biomarker distributions and compound specific isotopic signatures in sediments from sites on the Northern European continental margin that are characterized by a diffusive flux of methane. At all sites, the organic matter (OM) is predominantly derived from terrestrial higher plants, with subordinate abundances of algal biomarkers, but biomarkers for archaea and bacteria are also present. The co-occurrence of the archaeal lipids archaeol, sn-2-hydroxyarchaeol and 2,6,10,15,19-pentamethylicosane (PMI) with non-isoprenoidal glycerol diethers inferred to derive from sulfate-reducing bacteria (SRB) is similar to microbial biomarker assemblages observed at cold seeps. The archaeal and inferred SRB biomarker concentrations typically reach maxima close to the sulfate-methane transition zone (SMTZ), where archaeal biomarkers are depleted in 13C. The 16S rRNA gene sequences from the SMTZ of the Aarhus Bay sediment core indicate the occurrence of ANME-1 archaea, consistent with inferences derived from biomarker distributions. The observations suggest that AOM in these diffusive settings is mediated by consortia of archaea and bacteria similar to those found at many seep and methane hydrate sites around the world. © 2009 Elsevier Ltd. All rights reserved.


Luesken F.A.,Radboud University Nijmegen | Wu M.L.,Radboud University Nijmegen | Op den Camp H.J.M.,Radboud University Nijmegen | Keltjens J.T.,Radboud University Nijmegen | And 5 more authors.
Environmental Microbiology | Year: 2012

'Candidatus Methylomirabilis oxyfera' is a denitrifying methanotroph that performs nitrite-dependent anaerobic methane oxidation through a newly discovered intra-aerobic pathway. In this study, we investigated the response of a M.oxyfera enrichment culture to oxygen. Addition of either 2% or 8% oxygen resulted in an instant decrease of methane and nitrite conversion rates. Oxygen exposure also led to a deviation in the nitrite to methane oxidation stoichiometry. Oxygen-uptake and inhibition studies with cell-free extracts displayed a change from cytochrome c to quinol as electron donor after exposure to oxygen. The change in global gene expression was monitored by deep sequencing of cDNA using Illumina technology. After 24h of oxygen exposure, transcription levels of 1109 (out of 2303) genes changed significantly when compared with the anoxic period. Most of the genes encoding enzymes of the methane oxidation pathway were constitutively expressed. Genes from the denitrification pathway, with exception of one of the putative nitric oxide reductases, norZ2, were severely downregulated. The majority of known genes involved in the vital cellular functions, such as nucleic acid and protein biosynthesis and cell division processes, were downregulated. The alkyl hydroperoxide reductase, ahpC, and genes involved in the synthesis/repair of the iron-sulfur clusters were among the few upregulated genes. Further, transcription of the pmoCAB genes of aerobic methanotrophs present in the non-M.oxyfera community were triggered by the presence of oxygen. Our results show that oxygen-exposed cells of M.oxyfera were under oxidative stress and that in spite of its oxygenic capacity, exposure to microoxic conditions has an overall detrimental effect. © 2012 Society for Applied Microbiology and Blackwell Publishing Ltd.


Wu M.L.,Radboud University Nijmegen | Ettwig K.F.,Radboud University Nijmegen | Jetten M.S.M.,Radboud University Nijmegen | Jetten M.S.M.,Technical University of Delft | And 4 more authors.
Biochemical Society Transactions | Year: 2011

Biological methane oxidation proceeds either through aerobic or anaerobic pathways. The newly discovered bacterium Candidatus 'Methylomirabilis oxyfera' challenges this dichotomy. This bacterium performs anaerobic methane oxidation coupled to denitrification, but does so in a peculiar way. Instead of scavenging oxygen from the environment, like the aerobic methanotrophs, or driving methane oxidation by reverse methanogenesis, like the methanogenic archaea in sulfate-reducing systems, it produces its own supply of oxygen by metabolizing nitrite via nitric oxide into oxygen and dinitrogen gas. The intracellularly produced oxygen is then used for the oxidation of methane by the classical aerobic methane oxidation pathway involving methane mono-oxygenase. The present mini-review summarizes the current knowledge about this process and the micro-organism responsible for it. ©The Authors Journal compilation ©2011 Biochemical Society.


Wu M.L.,Radboud University Nijmegen | van Alen T.A.,Radboud University Nijmegen | van Donselaar E.G.,University Utrecht | Strous M.,MPI for Marine Microbiology | And 3 more authors.
FEMS Microbiology Letters | Year: 2012

'Candidatus Methylomirabilis oxyfera'; is a polygon-shaped bacterium that was shown to have the unique ability to couple anaerobic methane oxidation to denitrification, through a newly discovered intra-aerobic pathway. Recently, the complete genome of Methylomirabilis oxyfera was assembled into a 2.7-Mb circular single chromosome by metagenomic sequencing. The genome of M. oxyfera revealed the full potential to perform both methane oxidation and the conversion of nitrite via nitric oxide into oxygen and dinitrogen gas. In this study, we show by immunogold localization that key enzymes from both methane- and nitrite-converting pathways are indeed present in single M. oxyfera cells. Antisera targeting the particulate methane monooxygenase (pMMO) and the cd1 nitrite reductase (NirS) were raised and used for immunogold localization in both single- and double-labelling experiments. Our previous studies have shown that M. oxyfera does not develop pMMO-containing intracytoplasmic membranes as is observed in classical proteobacterial methanotrophs. Our results suggest that in M. oxyfera, the pMMO and NirS enzymes localized to the cytoplasmic membrane and periplasm, respectively. Further, double-labelling showed co-occurrence of pMMO and NirS in single M. oxyfera cells. © 2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved.


Roundworms and segmented worms and their bacterial symbionts, called Candidatus Thiosymbion. In the middle image, bacterial cells are colored green and host nuclei are stained blue. In the images on the right, symbionts are labelled “Ba”. Credit: MPI for Marine Microbiology If your favourite pub moves – would you move too or look for another pub? For bacteria living in symbiosis with marine worms it all depends on whether they sit outside or inside the pub. Scientifically speaking: bacteria living on the body surface of their hosts are loyal to those, while bacteria living inside their hosts prefer to stay local, as scientists from the Max-Planck-Institute for Marine Microbiology from Bremen now revealed. Nematodes and annelids. These are roundworms and segmented worms. They are just worms, one might think. "In fact, these two animal phyla are about as different as men and turtles", says Judith Zimmermann from the Max Planck Institute for Marine Microbiology in Bremen, Germany. "And yet they live in symbiosis with very closely related bacteria." The symbiotic tenants of roundworms and segmented worms belong to a group of closely related bacteria named Candidatus Thiosymbion. These bacteria supply their hosts with nutrition. In the roundworms – in a subfamily called Stilbonematinae -, they live on the body surface. "The bacteria cover the worm like a sleeping bag, only the head and the tip of the tail peek out", Zimmermann explains. In contrast, in segmented worms – in the gutless oligochaetes –, the bacteria live underneath the worms' skin and feed their host so well that they have lost their mouth and gut. "Our results show that these symbiotic bacteria appear to have switched multiple times between roundworms and segmented worms and accordingly between ecto- and endosymbiotic lifestyles during the course of their evolution", Zimmermann explains. "This flexibility is remarkable, because bacteria are generally adapted to one type of lifestyle and one group of hosts", adds Cecilia Wentrup who also participated in the study. "It was the large amount of data we analysed during this study that allowed us to reconstruct the closely interwoven evolution of these symbionts and their marine hosts." Outside and loyal or inside but fickle Despite their remarkable flexibility, however, the symbionts are very loyal to their hosts in some concerns. Once again, Zimmermann and her colleagues were in for a surprise. Contrary to the expectations of Zimmermann and her colleagues, the external tenants seem to show more long-term loyalty to their hosts than the internal cohabitants. "Long-term means over millions of years", Zimmermann clarifies. "The host-symbiont-relationship is very stable for the roundworms and their bacteria. Apparently, they have co-evolved with each other without changing their partner." Closely related roundworms were always associated with closely related symbionts. This high fidelity was seen in hosts from around the world, whether Zimmermann and her colleagues looked at roundworm-bacteria associations from Sylt, the Caribbean, the Mediterranean or Australia. The picture is different in the symbiosis between segmented worms and their bacteria. "Relationships were much less stable in these associations", Wentrup explains. "In the segmented worms, not only the host species plays a role." Rather, the location is also important. The researchers often found that distantly-related host species from the same geographic region had very similar symbionts. And vice-versa, closely related hosts from different geographic regions often had only distantly-related symbionts. "Closely related segmented worms from Australia and the Caribbean, for example, do not always have closely related symbionts", Wentrup adds. "This suggests that in the segmented worms, the original bacterial symbionts were often replaced by local bacteria". The results of this study clearly show how flexible and full of surprises marine symbioses are. "Next we plan to investigate what determines the lifestyles of these symbionts", says Nicole Dubilier, Director of the Department of Symbiosis at the Max Planck Institute for Marine Microbiology. Which factors decide whether the Candidatus Thiosymbion-bacteria remain external and attached to the surfaces of their hosts or become internal and live under the worms' skin? How do host and symbionts recognize each other? And do ectosymbionts become endosymbionts, or the other way round? This is what the Max Planck researchers want to find out in further studies. More information: Judith Zimmermann et al. Closely coupled evolutionary history of ecto- and endosymbionts from two distantly-related animal phyla, Molecular Ecology (2016). DOI: 10.1111/mec.13554


Monismith S.G.,Stanford University | Herdman L.M.M.,Stanford University | Ahmerkamp S.,MPI for Marine Microbiology | Hench J.L.,Stanford University | Hench J.L.,Duke University
Journal of Physical Oceanography | Year: 2013

Observations of waves, setup, and wave-driven mean flows were made on a steep coral forereef and its associated lagoonal system on the north shore of Moorea, French Polynesia. Despite the steep and complex geometry of the forereef, and wave amplitudes that are nearly equal to the mean water depth, linear wave theory showed very good agreement with data. Measurements across the reef illustrate the importance of including both wave transport (owing to Stokes drift), as well as the Eulerian mean transport when computing the fluxes over the reef. Finally, the observed setup closely follows the theoretical relationship derived from classic radiation stress theory, although the two parameters that appear in the model-one reflecting wave breaking, the other the effective depth over the reef crest-must be chosen to match theory to data. © 2013 American Meteorological Society.

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